Transposable element activity and polymorphisms drive structural variability within and between individuals in bivalves

Abstract

Structural variants (SVs) represent one of the most abundant sources of genetic variation across eukaryotes, with transposable elements (TEs) standing out as primary contributors in their emergence. While sequencing advances have highlighted the central role of SVs in generating genomic diversity, their contribution to adaptive evolution remains critically understudied, particularly in non-model invertebrates. Bivalves represent an ideal study system in this context due to their highly dynamic genomes and adaptation to diverse environmental conditions. Here, we use oysters as a model system to characterize how SVs and TEs reshape their genome and promote local adaptation. To achieve this, we leverage four publicly available assemblies, and we re-analyzed a large-scale dataset of the Estuarine oyster ( Crassostrea ariakensis ) collected across a wide range of different temperature and salinity conditions. We explicitly account for strengths and limitations of SV-calling software and benchmark our results through simulations. We uncover pervasive within-individual structural variability, with up to 14% of the oyster genome being affected by heterozygous INDELs. The strong enrichment of TEs within these SVs is driven by a prevalence of insertions over deletions, reflecting population-level TE activity. Strikingly, both SVs and de novo TE insertions — driven by the concurrent mobilization of diverse TE families — segregate among C. ariakensis populations and contribute to genomic differentiation potentially associated with local adaptations. Our study establishes oysters as a powerful framework for SV research and provides empirical evidence that SVs are an active evolutionary force generating potentially adaptive genetic variation in a key lineage of ecologically and economically important bivalves.